Chromosomal inversions can contribute to local adaptation by preventing recombination between co-adapted alleles. However, their central role in parallel evolution is not well understood. In this study, we investigate the contribution of chromosomal inversions to parallel evolution in the European flat oyster, Ostrea edulis. Previous studies suggested that parallel evolution in distant populations is associated with putative chromosomal inversions. However, due to limited marker density, finer-scale genomic regions reflecting parallel evolutionary signals have remained elusive. To address this gap, we used whole genome sequencing to analyze 35 oysters throughout the species range. Our analysis confirmed the presence of three polymorphic chromosomal inversions, two of which demonstrated a parallel pattern of differentiation. Interestingly, we also identified narrower signals of parallelism between genetic lineages throughout the genome, extending beyond the inverted regions. Demographic history analyses revealed a signal of secondary contact, suggesting that chromosomal inversions as well as the non-inverted islands of genetic parallelism retain a shared evolutionary history that has been erased by recent gene flow in the majority of the genome. Our findings indicate that while chromosomal inversions may play an important role in parallel evolution, other genomic regions may also be involved. Finally, these results may have implications for conservation management. The flat oyster is an economically important species that has experienced a large decline in population size due to overexploitation. Understanding the complex patterns of population structure in this species is crucial to inform translocations and other management actions.